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Age-related alterations of gastric mucosa and estrogen synthesis in rat parietal cells

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Abstract

The stomach has diverse functions other than gastric acid secretion. Multifaceted studies have investigated age-related changes of the gastrointestinal tract. Nevertheless, little is known about estrogen production changes in gastric parietal cells in rats aged over 3 months. We investigated age-related changes in gastric estrogen synthesis and the accompanying changes in liver estrogen receptor from 3 to 24 months. Weights of the body, stomach, and liver increased linearly from 3 to 18 months, then maintained a constant proportion up to 24 months. The gastric mucosa area (in mm2/1 mm muscularis mucosa) showed a constant proportion throughout the rats’ life. The population of parietal cells immunostained area with H+/K+-ATPase decreased gradually with advancing age. Cells that were immunopositive to aromatase antibody were observed at 3–24 months. The expressions of aromatase mRNA and its protein were somewhat lower at 18 and 24 months than at 3 months. The portal venous estradiol concentration at 12 months was 1.5 times higher than that at 3 months, and that at 18 months was a half of that at 3 months. The expression of estrogen receptor mRNA in the liver at 18 and 24 months was about 80% of that at 3 months. Results suggest that the gastric estrogen production declines with aging, and the liver estrogen receptor is also affected accordingly. Simultaneously, the gastric mucosa continues to express aromatase to maintain liver function(s) throughout the animal’s life.

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References

  • Altum M, Bergmn E, Edstrom E, Johnson H, Ulfhake B (2007) Behavioral impairments of the aged rats. Physiol Behav 92:911–923

    Article  Google Scholar 

  • Barsoum NJ, Gough AW, Sturgess JM, de la Iglesia FA (1984) Morphologic features and incidence of spontaneous hyperplastic and neoplastic mammary gland lesions in Wistar rats. Toxicol Pathol 12:26–38

    Article  CAS  Google Scholar 

  • Bloomfield AL, Keefer CS (1928) Gastric acidity: relation to various factors such as age and physical fitness. J Clin Invest 5:285–294

    Article  CAS  Google Scholar 

  • Caruso I, Porro GB (1980) Gastroscopic evaluation of anti-inflammatory agents. Br Med J 280:75–78

    Article  CAS  Google Scholar 

  • Elsborg L, Lung V, Bastrup-Madsen P (1976) Serum vitamin B12 levels in the aged. Acta Med Scand 200:309–314

    Article  CAS  Google Scholar 

  • Hollander D, Tarnawski A, Stachura J, Gergely H (1989) Morphologic changes in gastric mucosa of aging rats. Dig Dis Sci 34:1692–1700

    Article  CAS  Google Scholar 

  • Kobayashi H (2020) Estrogen synthesis in gastric parietal cells and secretion into portal vein. Anat Sci Int 95:22–30

    Article  CAS  Google Scholar 

  • Kobayashi H, Yoshida S, Sun YJ, Shirasawa N, Naito A (2013a) Gastric estrogen increases pituitary estrogen receptor α and prolactin mRNAs during the different pathological conditions of the liver. Endocrine 43:170–183

    Article  CAS  Google Scholar 

  • Kobayashi H, Yoshida S, Sun YJ, Shirasawa N, Naito A (2013b) Gastric E2 and liver ERα correlate to serum E2 in the cholestatic male rat. J Endocrinol 219:39–49

    Article  CAS  Google Scholar 

  • Kobayashi H, Yoshida S, Sun YJ, Shirasawa N, Naito A (2013c) Postnatal development of gastric aromatase and portal venous estradiol-17β levels in male rats. J Endocrinol 218:117–124

    Article  CAS  Google Scholar 

  • Kobayashi H, Yoshida S, Sun YJ, Shirasawa N, Naito A (2014) Changes of gastric aromatase and portal venous 17β-estradiol during the postnatal development and estrus cycle in female rats. Endocrine 46:605–614

    Article  CAS  Google Scholar 

  • Kobayashi H, Yoshida S, Sun YJ, Shirasawa N, Naito A (2016a) 17β-Estradiol in the systemic circulation derives mainly from the parietal cells in cholestatic female rats. J Endocrinol Invest 39:389–400

    Article  CAS  Google Scholar 

  • Kobayashi H, Yoshida S, Sun YJ, Shirasawa N, Naito A (2016b) Gastric 17β-estradiol in portal vein and liver Esr1 make a circadian rhythm in systemic circulation in male rats. Endocrine 53:565–573

    Article  CAS  Google Scholar 

  • Kobayashi H, Yoshida S, Shirasawa N, Maeda K, Naito A (2019) Expression and localization of aromatase in human gastric mucosa—immunohistochemical study using biopsy materials. Histochem Cell Biol 151:21–28

    Article  CAS  Google Scholar 

  • Kobayashi H, Shirasawa N, Naito A (2021) Estrogen synthesis in the stomach of Sprague Dawley rats: comparison to Wistar rats. Exp Anim 70:63–72

    Article  CAS  Google Scholar 

  • Kogire M, Ishizuka J, Parekh D, Greeley GH Jr, Thompson JC (1993) Effects of aging on gastrin and somatostatin secretion from isolated perfused rat stomach. Dig Dis Sci 38:303–308

    Article  CAS  Google Scholar 

  • Livak KJ, Schmitten TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Method 25:402–408

    Article  CAS  Google Scholar 

  • McGuigan JE, Trudeau WL (1970) Serum gastrin concentrations in pernicious anemia. N Engl J Med 282:358–361

    Article  CAS  Google Scholar 

  • Moshier JA, Cornell T, Majumdar AP (1993) Expression of protease genes in the gastric mucosa during aging. Exp Gerontol 28:249–258

    Article  CAS  Google Scholar 

  • Myers BM, Smith JL, Graham DY (1987) Effect of red pepper and black pepper on the stomach. Am J Gastroenterol 82:211–214

    CAS  PubMed  Google Scholar 

  • Nelson DR, Koymans L, Kamataki T, Stegeman JJ, Feyereisen R, Waxman DJ, Waterman MR, Gotoh O, Coon MJ, Estabrook RW, Gunsalus IC, Nebert DW (1996) P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics 6:1–42

    Article  CAS  Google Scholar 

  • Owen DA (1986) Normal histology of the stomach. Am J Surg Pathol 10:48–61

    Article  CAS  Google Scholar 

  • Snyder DL, Pollard M, Wostmann BS, Luckert P (1990) Life span, morphology, and pathology of diet-restricted germ-free and conventional Lobund-Wistar rats. J Gerontol 45:B52-58

    Article  CAS  Google Scholar 

  • Ueyama T, Shirasawa N, Matsuzawa M, Yamada K, Shelangouski M, Ito T, Tsuruo Y (2002) Gastric parietal cells: potent endocrine role in secreting estrogen as a possible regulator of gastro-hepatic axis. Endocrinology 143:3162–3170

    Article  CAS  Google Scholar 

  • Ueyama T, Shirasawa N, Ito T, Tsuruo Y (2004) Estrogen-producing steroidogenic pathways in parietal cells of the rat gastric mucosa. Life Sci 74:2327–2337

    Article  CAS  Google Scholar 

  • Vanzant FR, Alvarez WC, Eusternan GB (1932) The normal range of gastric acidity from youth to old age. Arch Intern Med 49:345–359

    Article  Google Scholar 

  • von Nesselrooij JH, Kuper C, Bosland MC (1992) Correlations between presence of spontaneous lesions of the pituitary (adenohypophysis) and plasma prolactin concentrations in aged Wistar rats. Vet Pathol 29:288–300

    Article  Google Scholar 

  • Waki S, Kinoshita Y, Wang HY, Asahara M, Matsushima Y, Hassan MS, Okada A, Maekawa T, Fukui H, Kawanami C, Kishi K, Chiba T (1998) Effect of aging on gastrin receptor gene expression in rat stomach. Peptides 19:225–229

    Article  CAS  Google Scholar 

  • Zhang W, Zheng SB, Zhuang Y, Xiang P, Xiao L, Li B, Ji DN, Xia SJ, Yu Z, Shi DY (2013) H+ /K+ ATPase expression in human parietal cells and gastric acid secretion in elderly individuals. J Dig Dis 14:366–372

    Article  CAS  Google Scholar 

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Acknowledgements

We are deeply grateful to all laboratory members for giving us constructive comments and warm encouragement.

Funding

This work was supported by JSPS KAKENHI Grant Number JP19K16470.

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Authors

Contributions

H.K. conducted experimental investigations and wrote the first draft of the manuscript. N.S. co-interpreted data and polished the manuscript. A.N. supervised the study. All authors contributed to and approved the final manuscript.

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Correspondence to Hiroto Kobayashi.

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The authors declare that no conflicts of interest exist that might prejudice the impartiality of this research work.

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All experiments were performed in accordance with institutional guidelines. All were approved by the animal research ethical committee of Yamagata University (#R3071).

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Kobayashi, H., Shirasawa, N. & Naito, A. Age-related alterations of gastric mucosa and estrogen synthesis in rat parietal cells. Histochem Cell Biol 157, 195–204 (2022). https://doi.org/10.1007/s00418-021-02054-0

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